Falconiformes, Accipitriformes, Strigiformes) in the Slovak Republic
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©2017 Institute of Parasitology, SAS, Košice DOI 10.1515/helm-2017-0038 HELMINTHOLOGIA, 54, 4: 314 – 321, 2017 New data on helminth fauna of birds of prey (Falconiformes, Accipitriformes, Strigiformes) in the Slovak Republic P. KOMOROVÁ1*, J. SITKO2, M. ŠPAKULOVÁ3, Z. HURNÍKOVÁ3,1, R. SAŁAMATIN4, 5, G. CHOVANCOVÁ6 1Department of Epizootology and Parasitology, Institute of Parasitology, The University of Veterinary Medicine and Pharmacy in Košice, Komenského 73, 041 81 Košice, Slovak Republic, *E-mail: [email protected]; 2Ornitological Station of Commenius Museum in Přerov, Bezručova 10, 750 02 Přerov, Czech Republic; 3Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic; 4Department of General Biology and Parasitology, Medical University of Warsaw, Chałubińskiego 5, 02-004 Warsaw, Poland; 5Department of Parasitology, National Institute of Public Health – National Institute of Hygiene, Chocimska 24, 00-719 Warsaw, Poland; 6Research Station and Museum of the Tatra National Park, 059 60 Tatranská Lomnica, Slovak Republic Article info Summary Received December 1, 2016 In the years 2012-2014, carcasses of 286 birds of prey from the territory of Slovakia were examined Accepted July 4, 2017 for the presence of helminth parasites. The number of bird species in the study was 23; fi ve belonging to the Falconiformes order, eleven to Accipitriformes, and seven to Strigiformes. A fi nding of Cestoda class comprehended 4 families: Paruterinidae (4), Dilepididae (2), Mesocestoididae (2) and Anoplo- cephalidae (1). Birds of prey were infected with 6 families Nematoda species of the Secernentea class: Syngamidae (1), Habronematidae (2), Tetrameridae (3), Physalopteridae (1), Acuariidae (1), and Anisakidae (2). Out of the Adenophorea class, the Capillariidae family (1) was confi rmed. The Acanthocephala group was represented by the Paleacanthocephala class, the Centrorhynchidae family (3). Out of the Trematoda class, 12 different species of fl ukes were found, belonging to the Diplostomidae (5), Cyathocotylidae (1), Strigeidae (4), Opistorchidae (1), and Plagiorchidae (1) fami- lies. The most frequent helminth species infecting diurnal birds of prey was Strigea falconis. This fl uke was confi rmed in one bird species from the Falconiformes order and in eight species from the Accipitriformes order. In nocturnal birds of prey, the most common fi nding was the acanthocephalan Centrorhynchus aluconis, identifi ed in four different host species of the Strigiformes order. In total, 23 helminth species were recorded for the fi rst time in Slovakia. Keywords: helminth parasites; infection; nocturnal and diurnal birds of prey Introduction Sanmartín et al. (2004), Illescas Gomez et al. (1993), and Santoro et al. (2012a, b). Birds of prey are predatory animals residing at the top of a food Forty-three different species of birds of prey, belonging to the Fal- chain and they usually get infected with parasites via ingestion of coniformes, Accipitriformes, and Strigiformes orders, nest or occur prey, thus serving as intermediate hosts of many parasite species. in Slovakia territory (Kovalik et al., 2010). The most abundant spe- Types and diversity of the prey preferred by individual species rep- cies is the common buzzard (Buteo buteo) that nests in different resent one of the factors affecting the parasite diversity in those forest biotopes, but it is very well adapted also to the agricultural hosts. land. However in low quantities, on the territory of Slovakia we can Since majority of birds of prey species in Europe are protected, the also fi nd the species that are very sensitive to the environmental research and knowledge of the parasite fauna is only fragmentary. changes associated with anthropogenic impacts (Circus pygargus, Comprehensive research projects studying all helminth groups in Milvus milvus) (Krivjanský, 2009). birds of prey were accomplished by the Borgsteede et al. (2003), In Slovakia, only two research papers, aimed at parasites in birds * – corresponding author 314 of prey, have been published in the 20th century. Tenora & Lusk minths, 17 out of 85 diurnal birds of prey from the Falconiformes or- (1960) and Škarda (1964) studied the helminth fauna of birds in der were infected (20 %), and the parasitic infection was confi rmed Czechoslovakia and published several fi ndings in birds of prey in 114 out of 156 birds from the Accipitriformes order (73.1 %). In from the Slovak part of the country. For a subsequent period of 50 nocturnal birds of prey (Strigiformes order), helminths were found years, at the times of dynamic climate changes, no comprehen- in 28 out of 45 individuals (62.2 %). sive research of this host group has been carried out. Recently, A total of 33 helminth taxa were registered. In the Falconiformes two papers on fl ukes and thorny-headed worms were published order, 9 different helminth taxa were determined – 2 Trematoda, 1 (Komorová et al., 2015; Komorová et al., 2016). Cestoda, 4 Secernentea, and 1 Paleacanthocephala. In birds from The aim of our study was to obtain the complex knowledge about the Accipitriformes order, in total 27 helminth species were found the current status of the parasite fauna in birds of prey in Slovakia. – 9 Trematoda, 6 Cestoda, 1 Adenophorea, 8 Secernentea, and 3 Paleacanthocephala. In nocturnal birds of prey (Strigiformes) 10 Material and Methods helminth species were detected – 2 Trematoda, 2 Cestoda, 1 Ad- enophorea, 4 Secernentea, and 1 Paleacanthocephala (Table 1). During the period of 2012 – 2014, 286 carcasses of birds of prey The information on parasite species, names and numbers of in- belonging to 23 species of the Falconiformes, Accipitriformes, and fected hosts (NIH), prevalence (P in %), intensity of infection (II), Strigiformes orders were examined for the presence of helminths mean intensity (MI), and site of infection is summarized below. (Table 1). The research was conducted upon the permission is- sued by the Ministry of Environment of the Slovak Republic No. Platyhelminthes 6467/2012-2.26467/2012-2.2. The samples were collected from Trematoda various locations of Slovakia in cooperation with departments Diplostomidae Poirier, 1886 of the State Nature Conservancy of the Slovak Republic – The Conodiplostomum perlatum (Ciurea, 1911) Slovenský Kras National Park, The Slovenský Raj National Park, Host: H. albicilla (NIH=1; P=100 %; II=43) – fi rst record in Slovakia The Pieniny National Park, The Regional Conservation Centre in Site of infection: small intestine Prešov, and The Vihorlat Protected Area, as well as with the Mu- seum of the Tatra National Park, the Clinic for Birds and Exotic Conodiplostomum spathula (Creplin, 1829) Animals at the University of Veterinary Medicine and Pharmacy Host: A. heliaca (NIH=1; P=16.7 %; II=13) – fi rst record in Slovakia in Košice, The Raptor Protection of Slovakia, The Rehabilitation Site of infection: small intestine Station in The ZOO Bojnice, and The Košice Airport. Collected bird carcasses were frozen and subjected to helminthological necrop- Neodiplostomum attenuatum (Linstow, 1906) sy. After de-freezing, all organ systems and body cavities were Host: B. buteo (NIH=29; P=24.4 %; II=1-224; MI=25), B. lagopus examined for the presence of parasites. Collected helminths were (NIH=1; P=20 %; II=70), B. rufi nus (NIH=2; P=50 %; II=6-10; washed in distilled water and preserved in 70 % ethanol. For mor- MI=8), P. apivorus (NIH=1; P=100 %; II=3) – fi rst records in Slo- phological identifi cation, the species belonging to the Trematoda vakia and Cestoda classes were stained with iron acetocarmine (Geor- Site of infection: small intestine giev et al, 1986). Lightening of specimens from the Adenopoho- rea, Secernentea, and Paleacanthocephala classes was carried Neodiplostomum canaliculatum (Nicoll, 1914) out using glycerine or lactophenol. The species identifi cation was Host: B. bubo (NIH=1; P=50 %; II=1), S. uralensis (NIH=5; conducted according to Dubois (1968, 1970), Gibson et al. (2002), P=33.3 %; II=5-23; MI=14) – fi rst records in Slovakia Sitko (1998, 2001), and Bray et al. (2008) for Trematoda; Joyeux Site of infection: small intestine & Timon-David (1934), Joyeux & Baer (1936), Rausch (1948), and Khalil et al. (1994) for Cestoda; Hartwich (1975), Baruš et al. Neodiplostomum spathoides Dubois, 1937 (1978), and Gibbons (2010) for Adenophorea; and Secernentea Host: B. rufi nus (NIH=1; P=25 %; II=4), C. aeruginosus (NIH=2; and Meyer (1933), Petrochenko (1958), Dimitrova et al. (1997), P=50 %; II=8-15; MI=11.5) – fi rst records in Slovakia and Dimitrova & Gibson (2005) for Paleacanthocephala. Ecologi- Site of infection: small intestine cal parameters (prevalence, mean intensity, diversity) were evalu- ated according to Bush et al. (2007). Cyathocotylidae Mühling, 1898 The voucher specimens are deposited in the collection of The In- Paracoenogonimus ovatus Katsurada, 1914 stitute of Parasitology at the SAS in Košice. Host: H. albicilla (NIH=1; P=100 %; II=1) – fi rst record in Slovakia Site of infection: small intestine Results Strigeidae Railiet, 1919 Out of 286 examined birds, 156 (54.5 %) were infected with hel- Parastrigea fl exilis (Dubois, 1934) 315 Table 1. List of birds of prey species investigated and nubmers of hosts infected with individual parasite classes. Order/bird species No. of birds parasitized by: No. of examined/ parasitized birds Tremtoda Cestoda Secernentea Adenophorea Paleacanthocephala Falconiformes 85/15 3 3 8 0 2 Falco cherrug Gray, 1834 3/2 - - 2 - - Falco columbarius L., 1758